On the neural substrates for exploratory dynamics in basal ganglia: A model

We present a neural network model of basal ganglia that departs from the classical Go/NoGo picture of the function of its key pathways-the direct pathway (DP) and the indirect pathway (IP). In classical descriptions of basal ganglia function, the DP is known as the Go pathway since it facilitates movement and the IP is called the NoGo pathway since it inhibits movement. Between these two regimes, in the present model, we posit that there is a third Explore regime, which denotes random exploration of the space of actions. The proposed model is instantiated in a simple action selection task. Striatal dopamine is assumed to switch between DP and IP activation. The IP is modeled as a loop of the subthalamic nucleus (STN) and the globus pallidus externa (GPe), capable of producing chaotic activity. Simulations reveal that, while the system displays Go and NoGo regimes for extreme values of dopamine, at intermediate values of dopamine, it exhibits a new Explore regime denoting a random exploration of the space of action alternatives. The exploratory dynamics originates from the chaotic activity of the STN-GPe loop. When applied to the standard card choice experiment used in the imaging studies of Daw, O'Doherty, Dayan, Seymour, and Dolan (2006), the model favorably describes the exploratory behavior of human subjects.

[1]  D. Plenz,et al.  A basal ganglia pacemaker formed by the subthalamic nucleus and external globus pallidus , 1999, Nature.

[2]  D. Sibley,et al.  Spatial learning deficit in dopamine D(1) receptor knockout mice. , 1999, European journal of pharmacology.

[3]  V. Srinivasa Chakravarthy,et al.  What do the basal ganglia do? A modeling perspective , 2010, Biological Cybernetics.

[4]  Charles J. Wilson,et al.  Activity Patterns in a Model for the Subthalamopallidal Network of the Basal Ganglia , 2002, The Journal of Neuroscience.

[5]  B. Averbeck,et al.  Effects of Dopamine Depletion on Network Entropy in the External Globus Pallidus , 2009, Journal of neurophysiology.

[6]  T. Maia Reinforcement learning, conditioning, and the brain: Successes and challenges , 2009, Cognitive, affective & behavioral neuroscience.

[7]  S. Johnson,et al.  Presynaptic dopamine D2 and muscarine M3 receptors inhibit excitatory and inhibitory transmission to rat subthalamic neurones in vitro , 2000, The Journal of physiology.

[8]  Peter A. Tass,et al.  Therapeutic rewiring by means of desynchronizing brain stimulation , 2007, Biosyst..

[9]  H. Yin,et al.  The role of the basal ganglia in habit formation , 2006, Nature Reviews Neuroscience.

[10]  Christopher G. Langton,et al.  Computation at the edge of chaos: Phase transitions and emergent computation , 1990 .

[11]  E Vorontsova,et al.  Motor and associative deficits in D2 dopamine receptor knockout mice , 2002, International Journal of Developmental Neuroscience.

[12]  Thomas P. Trappenberg,et al.  Modelling divided visual attention with a winner-take-all network , 2005, Neural Networks.

[13]  W. Schultz Predictive reward signal of dopamine neurons. , 1998, Journal of neurophysiology.

[14]  Peter Brown,et al.  Parkinsonian Beta Oscillations in the External Globus Pallidus and Their Relationship with Subthalamic Nucleus Activity , 2008, The Journal of Neuroscience.

[15]  Charles J. Wilson,et al.  Move to the rhythm: oscillations in the subthalamic nucleus–external globus pallidus network , 2002, Trends in Neurosciences.

[16]  J. Penney,et al.  The functional anatomy of basal ganglia disorders , 1989, Trends in Neurosciences.

[17]  G. Deuschl,et al.  Neuronal activity of the human subthalamic nucleus in the parkinsonian and nonparkinsonian state. , 2008, Journal of neurophysiology.

[18]  K. Sigvardt,et al.  Modeling facilitation and inhibition of competing motor programs in basal ganglia subthalamic nucleus–pallidal circuits , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Rafal Bogacz,et al.  Integration of Reinforcement Learning and Optimal Decision-Making Theories of the Basal Ganglia , 2011, Neural Computation.

[20]  C. Gray,et al.  Dynamics of tremor-related oscillations in the human globus pallidus: a single case study. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Shun-ichi Amari,et al.  Modeling Basal Ganglia for Understanding Parkinsonian Reaching Movements , 2010, Neural Computation.

[22]  T. Robbins,et al.  Effects of STN lesions on simple vs choice reaction time tasks in the rat: preserved motor readiness, but impaired response selection , 2001, The European journal of neuroscience.

[23]  J. Houk,et al.  Modulation of striatal single units by expected reward: a spiny neuron model displaying dopamine-induced bistability. , 2003, Journal of neurophysiology.

[24]  O. Hikosaka,et al.  Role of the basal ganglia in the control of purposive saccadic eye movements. , 2000, Physiological reviews.

[25]  Karl J. Friston,et al.  Dissociable Roles of Ventral and Dorsal Striatum in Instrumental Conditioning , 2004, Science.

[26]  Edward T. Bullmore,et al.  Broadband Criticality of Human Brain Network Synchronization , 2009, PLoS Comput. Biol..

[27]  F. Gonon Prolonged and Extrasynaptic Excitatory Action of Dopamine Mediated by D1 Receptors in the Rat Striatum In Vivo , 1997, The Journal of Neuroscience.

[28]  J. del R. Millán,et al.  Characterizing the EEG Correlates of Exploratory Behavior , 2008, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[29]  P. Dayan,et al.  Cortical substrates for exploratory decisions in humans , 2006, Nature.

[30]  Michael J. Frank,et al.  Dynamic Dopamine Modulation in the Basal Ganglia: A Neurocomputational Account of Cognitive Deficits in Medicated and Nonmedicated Parkinsonism , 2005, Journal of Cognitive Neuroscience.

[31]  David Terman,et al.  Transitions between irregular and rhythmic firing patterns in excitatory-inhibitory neuronal networks , 2007, Journal of Computational Neuroscience.

[32]  M. Frank,et al.  Striatal Dopamine Predicts Outcome-Specific Reversal Learning and Its Sensitivity to Dopaminergic Drug Administration , 2009, The Journal of Neuroscience.

[33]  V. S. Chakravarthy,et al.  The Role of the Basal Ganglia in Exploration in a Neural Model Based on Reinforcement Learning , 2006, Int. J. Neural Syst..

[34]  Hui Zhang,et al.  Heterosynaptic Dopamine Neurotransmission Selects Sets of Corticostriatal Terminals , 2004, Neuron.

[35]  Peter Brown,et al.  Complexity of subthalamic 13–35Hz oscillatory activity directly correlates with clinical impairment in patients with Parkinson's disease , 2010, Experimental Neurology.

[36]  G. E. Alexander,et al.  Functional architecture of basal ganglia circuits: neural substrates of parallel processing , 1990, Trends in Neurosciences.

[37]  Michael J. Frank,et al.  Genetic triple dissociation reveals multiple roles for dopamine in reinforcement learning , 2007, Proceedings of the National Academy of Sciences.

[38]  J. Bolam,et al.  Dopamine regulates the impact of the cerebral cortex on the subthalamic nucleus–globus pallidus network , 2001, Neuroscience.

[39]  C. Gerfen Molecular effects of dopamine on striatal-projection pathways , 2000, Trends in Neurosciences.

[40]  A Beuter,et al.  Dynamics of the Subthalamo-pallidal Complex in Parkinson’s Disease During Deep Brain Stimulation , 2008, Journal of biological physics.

[41]  D. Willshaw,et al.  Subthalamic–pallidal interactions are critical in determining normal and abnormal functioning of the basal ganglia , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[42]  Eytan Ruppin,et al.  Actor-critic models of the basal ganglia: new anatomical and computational perspectives , 2002, Neural Networks.

[43]  M. Frank,et al.  Prefrontal and striatal dopaminergic genes predict individual differences in exploration and exploitation. , 2009, Nature neuroscience.

[44]  Akinori Akaike,et al.  Excitatory and inhibitory effects of dopamine on neuronal activity of the caudate nucleus neurons in vitro , 1987, Brain Research.

[45]  R. Krishnan,et al.  Modeling the role of basal ganglia in saccade generation: Is the indirect pathway the explorer? , 2011, Neural Networks.